Ødegaard & Frame • Generalist flowers and in tropical trees TAXON 56 (3) • August 2007: 696–706

Generalist flowers and phytophagous beetles in two tropical canopy trees: resources for multitudes

Frode Ødegaard1 & Dawn Frame2

1 Norwegian Institute for Nature Research (NINA), Tungasletta 2, 7485 Trondheim, Norway. [email protected] (author for correspondence) 2 Herbarium, Institut de Botanique, 163 rue A. Broussonnet, 34090 Montpellier, France

In the Republic of Panamá, phytophagous beetles were collected by hand and beating from superficially similar generalist blossoms of Nectandra umbrosa (Lauraceae) and Tapirira guianensis (Anacardiaceae), two phylo- genetically distant Neotropical canopy trees. Beetles were sorted into three functional groups (guilds): general flower visitors, species developing in buds, and seed predators. Out of a total of 1,564 collected specimens belonging to 177 species, 55 species or 31% were identifiable to specific epithet. These small- to medium- sized beetles belonged to four families: Cerambycidae, Chrysomelidae, Brentidae, and . A total of 723 beetles representing 121 species, and 841 beetles representing 121 species were recorded from N. umbrosa and T. guianensis, respectively. Of the beetles collected, 65 species were common to both trees, which equates to a similarity index value of 0.46 (Jaccard) or 0.34 (Sørensen). With respect to functional groups, there was no significant difference in the number of beetle species between the two tree species. Overall, beetle abundance patterns on flowers of the two trees are similar in terms of phytophagous beetle subfamily dominance. There are differences however, significantly more leaf beetles (Cryptocephalinae, Eumolpinae, Galerucinae) were collected per hour on T. guianensis than on N. umbrosa. Moreover, among beetles shared between the two tree species, Baridinae weevils showed a tendency to be more abundant on N. umbrosa. Nearly three-quarters of the flower feeders (72%) were shared between the two trees. The large overlap in beetle species between the two plant species suggests that the fauna is fairly general in terms of host use. We discuss the possible significance of our results to phytophagous beetle and host plant evolution. The combined effects of large species numbers, high abundance and broad diet breadth across generalist flowers of tropical canopy trees suggests that small- to medium-sized beetles play a crucial role in maintenance of species biodiversity and forest ecosystem function.

Keywords: canopy, Coleoptera, florivory, Panama, tropical forests

There has been little field research directed at un- INTRODUCTION derstanding the interplay between phytophagous beetles Overall, the greatest species diversity on Earth is and generalist flowers, the most notable exception being found in tropical forests, and this is true for both phy- Kirmse & al. (2003). For the purposes of our discussion, tophagous beetles and angiosperms. The most speciose a generalist flower is one that has an open morphology organisms are , and recent estimates suggest and allows access to a diversity of visitors, such that there are 7 to 10 million species (Ødegaard, 2000a, flowers typically have more visitors than principal pol- 2006; Novotny & al., 2002); such estimates are usually linators (Frame, 2003). Studies of visitors to generalist based on extrapolations from herbivory studies and the flowers in the tropics are rare, probably because of the different values obtained relate to the hypothetical per- difficulties associated with identifying the numerous and centage of generalist feeders, the greater the proportion varied from different orders, many of which may of generalists, the lower the estimated value of arthropods be undescribed or lack recent revisionary treatment or (Erwin, 1982; Ødegaard, 2000a). Phytophagous beetles for which no taxonomist exists. With respect to beetles in are thought to be the most species-rich group and they general, Bernhardt (2000) writes “From the entomological are estimated to represent 700,000 to 1 million species, or perspective, the taxonomy of most Coleoptera is so poorly about 20% of all arthropods (Ødegaard, 2000a). Vascular understood that it is often impossible to identify flower- plants represent another species-rich higher order group visiting specimens beyond the level of subfamily…” Gen- with about 400,000 species, the great majority of which eralist flowers are often described by biologists as having are angiosperms (May, 2000). So, we have an intriguing many small visitors and left at that. relationship between the most speciose organisms, phy- Strong & al. (1984), among others, have defined tophagous beetles, and vascular plants, their hosts. phytophagous insects as those insects that feed on living

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tissue of higher plants; this narrow definition includes leaf-, tinguish and identify the collected specimens. Our study flower-, and fruit-eaters, but excludes algae-, moss-, and represents one of the few quantitative studies of beetle lichen-feeders, granivorous species and wood-borers. A visitors to generalist flowers of the tropical canopy. broader, possibly more realistic concept such as that of Ødegaard (2000b) includes all plants and dead plant tissue (such as wood). Strict adherence to the first definition is problematic; for instance, wood-borers (xylophages) feed MATERIALs and METHODS mainly on dead plant tissue as larvae, however, many of Site. — The study was carried out in an evergreen, these insects are regularly attracted to flowers as adults wet Panamanian lowland forest in San Lorenzo Protected where they feed on living plant tissue. Florivory is a form of Area (9°17′ N, 79°58′ W, ca. 130 m a.s.l.), Colon province, phytophagy wherein feed on flowers. With respect 4.4 km inland from the Atlantic coast. Average annual to beetle specialists, they may feed either as adults, larvae, temperature and precipitation is 25.8°C and 3,140 mm, or both. Florivorous insects may be important pollinators respectively. There is a pronounced dry season from for their host plants (Endress, 1994). Frame (2003) has mid-December to the end of April; at this time the forest argued that flower eating is just a form of herbivory and receives about 10% of its yearly precipitation. The forest that this is a fundamental phenomenon—pollination, as is dominated by 35 to 45 m tall trees; lianas and epiphytes one possible outcome of florivory, therefore, is secondary. occur regularly in the canopy. The San Lorenzo Protected The issue of whether florivores are “principal” pollinators Area includes 9,600 ha of relatively old-growth tropical may, therefore, be irrelevant in some contexts. forest that has escaped anthropogenic disturbance for It is believed that beetles are guided to flowers by about 200 years (Basset & al., 2003). certain cues, especially color (see Waser, 1983) and scent The canopy was reached using a 54 m tall crane hav- (Gottsberger, 1989). As pointed out by Forel (1910), color ing an arm length of 55 m. The projected area accessible forms a cue for insects but has no attraction in and of for study is 0.88 ha. Within the crane perimeter there are itself, and color displays by blossoms (flowers or aggrega- ca. 40 tree species and ca. 35 species of climbers that can tions of flowers, e.g., inflorescences) may be important for be reached from the gondola. There are two individuals beetles as a form of “advertisement” (Waser, 1983). Cues of Nectandra umbrosa, a short canopy tree, and several aid beetles to orient themselves within their environment, individuals of Tapirira guianensis, a surmounting tree. and those cues which lead beetles to food and/or mates, There was a minimum distance of 10 m between study result in what we, as observers of the phenomenon, call trees and 20 m between conspecific trees. At the site, “attraction”. T. guianensis flowers first, followed about a week or so We studied phytophagous beetle visitors to super- later by N. umbrosa ; there is no overlap in flowering ficially similar generalist flowers and inflorescences of between the two species. two phylogenetically distant canopy trees, Nectandra Plants. — Here follows a detailed description of umbrosa (Lauraceae) and Tapirira guianensis (Anacar- the study plants with an emphasis on the flowers, a brief diaceae), in order to document species composition of the summary of floral and inflorescence characters likely phytophagous beetle fauna found there. This information to be relevant to small beetle attraction are presented in was subsequently analyzed with respect to beetle diversity Table 1. and functional groups and used as a basis of comparison between the two trees. This pilot study was carried out Nectandra umbrosa (Lauraceae) (Fig. 1A–B) as part of a wider study of beetle diversity by the first Tree to 25 m growing from Honduras south to Co- author (Ødegaard, 2006) at the San Lorenzo Protected lombia, often found below 50 m altitude in rainforests and Area, Republic of Panama using the Smithsonian Tropical beach thickets, or even secondary forest. Inflorescences Research Institute (STRI) canopy crane located at this site. lateral near apex of branches, emergent above leaf can- The beetle fauna of this region is relatively well known opy. Seen from a distance, inflorescences appearing as an compared to the rest of the tropics, permitting us to dis- irregularly undulating white carpet, each inflorescence

Table 1. Comparison of selected floral and inflorescence characters potentially relevant to beetle visitors to Nectandra umbrosa and Tapirira guianensis. Attractivity of Flower diameter Petal or tepal Stamen length in mm/ Inflorescences in in mm number/color/ shorter or equaling Nectar/ days (height) (petals/tepals) pubescent petals-tepals scent Nectandra umbrosa 21 (7) 5 (2.5) 6/white/yes To 1.0/shorter Yes (3 glands)/sweet Tapirira guianensis 7 (3) 2.5 (1.2–1.5) 5/white/yes To 1.5/equaling Yes (interstaminal disk)/sweet musky

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Fig 1. Flowers of Nectandra umbrosa and Tapirira guianensis. A, N. umbrosa as seen from the STRI canopy crane, San Lorenzo Protected Area, Panama (Photo: F. Ødegaard); B, close-up of flowers (Photo: S. Paton); C, T. guianensis as seen from canopy crane (Photo: F. Ødegaard); D, unisexual flower of T. guianensis from a dioecious tree, Recife, Brazil (Photo: L. Krause). up to 13 cm long. The small flowers (5 mm) are usually of the third whorl bear two globose glands at their base, disposed in clusters of 2 to 10 or more on short branches which secrete minute amounts of nectar. Stamens upright, mostly arising from secondary inflorescences axes, over- appearing as a small crown, not quite one-third the length all shape of inflorescences hemispherical. Pedicels (to of the tepals. Anthers each having 4 half-thecae, opening 0.6 mm) hirsute, bearing flowers with 6 white adaxially by broadly elliptical flaps; when dehiscent appearing papillose, horizontally spreading, ligulate in outline te- brilliant yellow because of the pollen. Gynoecium ca. pals, arranged in two whorls of three, each about 2.5 mm 1 mm long, hirsute ovary globose to plumply ellipsoid long and 0.6–1.0 mm wide. Androecium composed of four terminated by a short style. Flowers sweet-smelling? Each whorls, the outer two have 3 stamens each as does the third flower lasts 1–2 days. In Nectandra, flowers are bisexual whorl, which has extrorse locules; the inner (fourth) whorl but dichogamous; there is a distinct female and male phase alternates with the third and is staminodial, much reduced separated temporally by a short dormant period (Henk van and appears as small cylindrical threads. All stamens and der Werff, pers. comm.). Usually flowers are protogynous, staminodia are inserted opposite the tepals. The stamens i.e., are functionally female first.

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Tapirira guianensis (Anacardiaceae) (Fig. 1C–D) eral manner, few additional beetle species were collected Tree to 35 m or more, growing from Honduras south at this period. For this reason, there was no night sampling to Bolivia in the west, through Paraguay to Santa Cata- of the two study tree species. The greatest yield of bee- rina, Brazil in the east; common in Amazonia and the tles was found to occur from 07:30 to 10:00, and so most Guianas. A widespread polymorphic species of the New sampling was done at this time. Two trees of each species World tropics, equally at home in lowland wet rainforest, were chosen and visited about twice a week during the lower montane forests and cerrado. Paniculate inflores- flowering period (here, the period when flowers attracted cences lateral near apex of branches, emergent above leaf beetles), which lasted from mid-April to the start of May canopy. Seen from a distance, inflorescences appear as (about 3 weeks) for T. guianensis and from the beginning white, broadly tapering masses about 250 cm long. The of May until early June (about 5 weeks) for N. umbrosa. In minute (2 mm) flowers are disposed singly or in clusters total, 5 and 8.5 hours were spent sampling inflorescences of up to 7–8 flowers on short branches mostly arising of T. guianensis and N. umbrosa, respectively. from secondary inflorescence axes. The near orthotropic Beetles were identified whenever possible to genus inflorescence axes become longer as they approach the and species, unidentified species were denoted sp. 1, sp. 2, branch apex. On expanded inflorescences, flowers are lo- etc. Most beetles were dissected to expose genitalia; many cated on the distal three-quarters of the axes. The hirsute species recognizable by this means were undescribed. pedicels (to 0.7 mm) elongate as the floral buds mature. Whenever it was unclear if the specimen represented a The connate, yellow, sparsely hirsute 5-lobed sepals are new species or genus, the taxon to which it resembled is leathery and alternate with the 5 free petals. The strongly given followed by a question mark (?). A list of all taxa can concave ovate liquid-filled petals are 1.2–1.5 mm long be found in the Appendix. Specimens are deposited in the and 0.7–1.0 mm at their widest point. The ten equal free collection of the first author at the Norwegian Institute for stamens are inserted opposite the sepals and petals below Nature Research (NINA, Trondheim). The species were the spongy intrastaminal disk, those opposite the sepals assigned to three functional groups (guilds) on the basis of maturing first. Mature stamens (to 1.5 mm), more or known biology for the genus: general flower visitors (F), less equaling the petals. The small versatile anthers are species developing in buds (FB) and seed predators (FS). sagittate, dehiscing to expose the pale yellow translucent Data analyses. — After a general characterization pollen. The pale yellow moist spongy intrastaminal disk of the collected beetles, we analyzed the beetle data from (1.0 mm in diameter) is more or less 10-lobed, the notches the two trees with respect to functional group and di- corresponding to the sites of filament insertion. Ringing versity (richness and abundance). Species overlap was the style and growing on it, are short hairs. The central measured as presence/absence data using the Sørensen- style appears as a five-pointed star, the points opposite and the Jaccard-index (Magurran, 2004). Statistical test- the petals; it is just emergent above the intrastaminal disk. ing for comparisons between the trees was carried out Besides the hairs along the style, the tips of which reach using the software SPSS 12.0 (LEAD Technologies, Inc., to the edges of the moist stigma, there is a central core of Chicago). hairs between the stigma lobes. Flowers give off a sweet musky scent and are open a single day. Inflorescences are in flower 3–7 days, with the height of flowering, that is, the greatest number of flowers open at the same time, RESULTS lasting about 1–3 days. At our site the flowers appeared to Out of a total of 1,564 specimens belonging to 177 be bisexual (pollen was present in anthers but we do not phytophagous beetle species collected, 55 species or 31% know if it is viable—it may function as “fodder” pollen), were identifiable to specific epithet. All beetles belong and all T. guianensis trees in the crane perimeter set fruit; to families recognized as having many flower-visiting however sexuality in this species appears to be unstable, species: Cerambycidae, Chrysomelidae, Brentidae, and and in other parts of its range, it may be dioecious (north Curculionidae. Table 2 provides a brief description of of Recife, L. Krause, pers. comm.). life-history characters and adult size of beetles from the different subfamilies. Beetle sampling and processing. — Phytophagous The total number of phytophagous beetles from all beetles of the Chrysomeloidea and Curculionoidea were functional groups is presented in Table 3. Insect surveys collected from Nectandra umbrosa and Tapirira guianensis from the tropics always include a high proportion of inflorescences by hand and beating over two consecutive species represented by a single specimen, known as a flowering seasons (2001–2002). Each sampling lasted 30 “singleton” (Novotny & Basset, 2000). The percentage of minutes per tree and took place between 06:30 and 18:15. singletons gives an indication of sampling completeness The first author (FØ) conducted night sampling on many (Magurran, 2004). Our collection yielded 31% singletons trees within the crane perimeter, and found that in a gen- which may be considered very good for invertebrate sam-

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Table 2. General characteristics related to life history of the study beetles. Size of adults in mm Family Subfamily (excluding antennas) Larval hosts Adult hosts Brentidae Brentinae 5–7 Woodborers/feed on wood Many spp. attracted to flowers fungi

Cerambycidae Cerambycinae 6–35; mostly 8–20 Woodborers Many spp. attracted to flowers, pollen feeders Lepturinae 6–20; mostly 8–15 Develop in rotten wood Attracted to flowers, pollen feeders

Chrysomelidae Cryptocephalinae 1–8; mostly 2–5 Develop in soil/feed on Flowers/young shoots and leaves detritus Eumolpinae 2–10; mostly 3–5 Develop in soil/feed on roots Flowers/leaves Galerucinae 2.5–10; mostly 6–9 Some spp. with free living Flowers/leaves phytophageous larvae; others in soil/feed on roots?

Curculionidae Baridinae 1–8; mostly 2–5 Various tissue/woodborers Flowers Curculioninae 1–5; mostly 2–3 Tribus Anthonomini develop In flowers, frequently on the in flower buds same as their larval host plants Tribus Derelomini associated with various tissues of monocots

Table 3. Total number of phytophagous beetles from all functional groups. Species Individuals Shared Shared singletons Unique singletons Nectandra umbrosa F 98 644 50 32 20 FB 6 7 4 5 2 FS 17 72 11 8 4 Total 121 723 65 45 26 Tapirira guianensis F 95 782 50 38 22 FB 9 16 4 6 3 FS 17 43 11 8 4 Total 121 841 65 52 29 Abbreviations: F, general flower visitors; FS, seed predators; FB, species developing in buds. ples from tropical forests as many studies report more than 50% (e.g., Kirmse & al. 2003). A total of 723 beetles representing 121 species, and 841 beetles representing 121 species were recorded from N. umbrosa and T. guianensis, respectively. Evidently, T. guianensis showed a stronger attraction rate for beetles than N. umbrosa (paired t-test: z = –2.87, p = 0.021). Of the

collected beetle species, 65 were common to both trees, Species number which equates to a similarity index value of 0.46 (Jaccard) or 0.34 (Sørensen). With respect to functional groups, there was no significant difference in the number of beetle species between the two plant species (F: paired t-test: z = –1.80, p = 0.36; FB: paired t-test: z = –2.17, p = 0.15; FS: paired t-test: z = 0.03, p = 0.51) (Fig. 2). Fig 2. Beetle species by functional group (guild). F, general Beetle abundance patterns on flowers of the two trees flower visitors; FB, species developing in buds; FS, seed are similar in terms of subfamily dominance (Fig. 3). predators; Nu, Nectandria umborsa ; Tg, Tapirira guianensis.

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Fig 3. Abundance of general flower feeders (abundance per collecting hour) of Nectandra umbrosa (Nu) and Tapirira guianensis (Tg) as a function of beetle subfamilies.

Fig 4. Abundance of general flower feeders (abundance per collecting hour) common to both Nectandra umbrosa (Nu) and Tapirira guianensis (Tg) as a function of beetle subfamilies.

However, with respect to detail there are some pronounced differences that merit mention. Significantly more leaf DISCUSSION beetles (Cryptocephalinae, Eumolpinae, Galerucinae) Taking into account the relatively small sampling were collected per hour on T. guianensis than on N. um- effort (13.5 h), species richness and abundance of phy- brosa (Paired t-test: z = –2.95, p = 0.016). On the other tophagous beetles are extremely high in flowers of the hand, among beetles shared between the tree species, study trees, and up to an order of magnitude higher than Baridinae weevils showed a tendency to be more abundant results obtained from studies of leaf chewers on individual on N. umbrosa (Fig. 4) (Paired t-test: z = –2.38, p = 0.086). trees using similar methods (e.g., Basset, 1990; Ødegaard, Nearly three-quarters of the flower feeders (72%) were 2000b; Barrios, 2003). Clearly, generalist flowers support shared between the two tree species. a very high species diversity of phytophagous beetles in

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tropical forests. Although we were not specifically inves- species, Cupania scrobiculata, at our study site also tigating beetle-pollination, it is evident that some pollen indicates that the latter species, more closely resembles transfer between conspecific trees must occur given this that of Nectandra umbrosa and Tapirira guianensis, while number of beetles. In a study of insect visitors to two Tachigali guianensis attracted a different beetle fauna and canopy trees in a Mata Atlantica forest fragment north of overall fewer beetles; a total of 92 beetle species were Recife, Brazil, Krause & Gottsberger (2005) found pollen recorded from the flowers of C. scrobiculata whereas on beetle visitors to female flowers of Tapirira guianensis only 14 from Tac. guianensis given the same sampling (dioecious at this site), and they consider beetles to be a effort (Ødegaard, unpub. data). It is therefore possible that pollinator of this species; such data challenges the view Tac. guianensis is much less of a generalist beetle flower that beetle-pollinated canopy trees are rare in lowland than a generalist, strongly bee-dominated one. It is also Neotropical wet forests (Bawa & al., 1985); the afore cited possible that seasonal and regional differences in insect researchers nevertheless concede that pollination studies fauna play a role and this may explain differences in the within this vegetation are biased towards large-flowered observed beetle fauna between Tac. guianensis and the species. The issue of whether common flower visitors other study trees. are pollinators is a tricky one (see Waser & al., 1996), it An interesting difference between the study trees is may very well be true that beetles are not always the most that more generalist leaf beetles (Chrysomelidae) were efficient of pollinators (especially in generalist systems) collected from Tapirira guianensis, than Nectandra um- even if they are often the first to arrive, but given their brosa. Conversely, the opposite is true with respect to richness and abundance in our study trees, they are likely Baridinae weevils. Regarding these differences, we have to contribute to pollination, even if bees, which are uni- to keep in mind that the datasets of this pilot study were versal tropical canopy flower visitors (to greater or lesser not large enough to test if infraspecific variation in beetle degrees), are very efficient pollen collectors and have the load within trees differed significantly from between tree ability to move quickly between trees. In any case, the species variation. Future studies should, therefore, include contribution to pollination of generalist flowers by various several trees of each species and blossom size should be insect visitors is likely to vary considerably with respect quantified. However, results from a broader study of 50 to space and time (see, e.g., Herrera, 1988; Waser & al., plants in the same area indicate that attractiveness of 1996; and references therein). It is an inescapable fact canopy trees and lianas bearing small white generalist that whether or not beetles pollinate, canopy flowers in flowers clustered in large inflorescences may be different, generalist flower systems represent an important source both in terms of general and differential attraction rate of food and a meeting place for individuals. For the pur- across beetle groups and that, among other things, this poses of this paper, we will assume that most of the beetle may relate to beetle life history (Ødegaard, 2006). Other “general flower visitors” were at the very least, rare to trees and lianas within the crane perimeter having small occasional pollinators of the study trees even if we did white flowers clustered in large inflorescences that seem not check for pollen. to be especially attractive to the Baridinae include the Our results indicate that phylogenetically distant sapindaceous canopy lianas Serjania mexicana and Paul- plants bearing superficially similar flowers and inflo- inia fibrigera, and the canopy trees Cupania scrobiculata rescences can attract the same groups (subfamilies) of (Sapindaceae) and Humiriastrum diguense (Humiriaceae) beetles. This was not the conclusion arrived at by Kirmse (Ødegaard, data not shown). & al. (2003) studying beetle visitors to the canopy trees In a review/theoretical article, Bernhardt (2000) traces Matayba guianensis (Sapindaceae) and Tachigali guian- beetle pollination modes and other phenomena along and ensis (Caesalpiniaceae) in Venezuela; they write “The across phyletic lines, and presents a classification system similarity of the beetle fauna among the tree species was for beetle pollination recognizing four overlapping mor- low despite a comparable structure of flowers.” There are phological modes: Bilabiate, Brush, Chamber Blossoms several possible reasons for the observed differences, the and Painted Bowl. He goes on to say beetle pollination flowers may have been more different than they took them modes are determined by suites of evolving characters to be. Tachigali guianensis had fewer beetles overall and but that there are distinguishable patterns, for example, the fauna was dissimilar to that of Matayba guianensis, biogeographical, e.g., Brush and Chamber Blossoms which at the level of beetle subfamily more resembled our predominate in the wet tropics. Bernhardt explains that study plants. The Tachigali is likely to be very attractive many flower-beetle patterns are the result of convergent to bees, as are most members of its family, and this is evolution, a logical conclusion based on existing evidence. certainly indicated by Kirmse & al.’s (2003) mention that Indeed, one of the pivotal issues in coleopteran system- its flowers produce a strong sweet scent. Unpublished atics and evolution is host lability. Blossoms of both of data of the first author respecting the flower beetle fauna the trees we studied are Brush—they “usually consist of of Tachigali guianensis and a different sapindaceous many, small, often unisexual flowers with reduced, or

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absent perianth segments massed together but devoid of son to suspect this and found beetle activity to be greatest overarching-enveloping bracts at the time when anthers from 07:30 to 10:00, suggesting that temperature, whatever dehisce and stigmas are receptive” (Berhardt, 2000). the source, was sufficient during this period. Interestingly, Morphologically-speaking, the inflorescences of Bernhardt (2000) holds that Chamber Blossoms attract the Nectandra umbrosa and Tapirira guianensis are func- greatest diversity of beetles although it is unclear what he tioning as flowers; it has been suggested that in beetle- means by diversity. This proposition may be true at the pollinated plants, aggregations of small, few-staminate family level, however, our data would argue that in terms flowers act to produce a multi-staminate condition in the of beetle genera and species, Brush Blossoms attract the blossom (Bernhardt, 2000) as polyandry is characteristic greatest diversity. Moreover, the number of beetle Brush of beetle-pollinated systems (Gottsberger, 1977; Bern- blossoms has been greatly underestimated (see estimates hardt & Thien, 1987). We observed general flower feeders in Bernhardt, 2000), presumably because of the paucity of to feed on pollen and, although small amounts of floral studies focussing on beetle visitors to generalist flowers nectar are available in both species, we suspect that the of lowland tropical wet forest canopy trees. principal food was pollen. The largest phytophagous bee- Both pollen feeding and nectar drinking are common tles collected were about 8–20 mm long (Cerambycidae) among phytophagous beetles; pollen provides comple- while members of other subfamilies were less than this mentary proteins to a beetles’ diet and nectar is rich in (Table 2), and about the size or smaller than an individual sugar and a source of amino acids (Jolivet & Hawkes- flower. The cerambycids frequently formed clouds above wood, 1995). Generalist phytophagous beetles, which are the inflorescences and would settle on blossoms to feed herbivores on numerous different plants, such as many on pollen and mate (F. Ødegaard & D. Frame, pers. obs.). Chrysomelidae, are often facultative florivores, feeding Although long, these beetles are slender and easily moved on pollen and nectar or other tissues (Samuelson, 1994; between flowers on inflorescences. It is recognized that Held & Potter, 2004). Other generalist chrysomelids may the physical size of such inflorescences, encourages con- be restricted to petals and other flower parts, yet without specific beetle interactions (as meeting and copulating great specificity possibly because of a parallel lack of sites) and beetle-flower ones possibly leading to pollen profound chemical specificity of corresponding tissues. deposition and transfer to receptive stigmas (Bernhardt, Oviposition in buds and flowers is common among 2000). Inflorescences composed of small flowers, as in many Anthonomini and Baridinae (Burke, 1976), respec- our study plants, provide a large surface area and diverse tively; the resulting larvae develop at the site. Such rela- topography, which may be important for beetle circulation tionships imply specialized factors for host recognition. and spatial segregation (see Frame & Durou, 2001). It Hence, it is likely that there are subtle chemical differen- is significant that the stamens are included or equal the ces among generalist flowers, yet to be discovered, which petals (Table 1), and so easily reachable by small beetles; determine the composition of the beetle fauna attracted well-exerted stamens in dense aggregated blossoms are to them (see also Bernhardt, 2000). Our findings that better manipulated by other sorts of animals, e.g., bees there may be different attraction rates of phytophagous and mammals. beetles even among generalist flowers (Fig. 3) would tend Bawa & al (1985) conclude, and we concur (for rea- to support this idea. sons given below), that there are fewer sorts of pollination With respect to beetle functional groups, the study systems in the canopy. Tree canopies are exposed habitats, plants were practically identical, suggesting that these during the day they can be hot, dry and receive high solar plants offer the same kind of resources for beetles. It is insolation (Parker, 1995). Canopy flowers may represent a common phenomenon that functional groups (guilds) small oases to beetles and other animals. It seems likely remain more or less constant, but species change over that there are a limited number of blossom forms in the space and time (Strong & al., 1984; Ødegaard, 2006). This canopy—partly related to the biophysical conditions found would seem to be true for both the flowers/inflorescences there—among the most common are large trumpet flowers (as morphological guilds) as well as the beetles, that is, (usually oriented perpendicular to mid-day sun) and clus- the flowers are functionally similar in terms of general ters of many small flowers (variously oriented, but some- attractivity to beetles but the plants are not closely related. times parallel to mid-day sun). We speculate that the latter, In this instance, floral bauplan is convergent and may dissected form (as in our study plants) is likely to disperse reflect the organization and evolution of beetle nervous heat efficiently and depending on flower pigmentation, systems’ as “blossom”-beetle interaction is a reciprocal may also reflect ultra-violet light. Large flowers are also relationship (see also Silberbauer-Gottsberger & al., 2001). thought to be good at dispersing heat (see Dieringer & al., Thus, theoretically, insect neurology should provide clues 1999). There exist temperature optima for beetle species to the interpretation of floral characters. and some beetle-flowers are thermogenic, possibly consti- The large overlap in beetle species between the two tuting a “reward” (Seymour & al., 2003). We have no rea- plant species suggests that the beetle fauna is fairly gen-

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eral in term of host use. Kirmse & al. (2003) report a lower tion of beetle-pollinated angiosperms. Pl. Syst. Evol. 222: overlap (Sørensen-index: 0.25 compared with ours 0.34), 293–320. but their proportion of singletons was higher, probably Bernhardt, P. & Thien, L. 1987. Self-isolation and insect pol- due to their predominate use of traps, which normally lination in the primitive angiosperms: new evaluations of older hypotheses. Pl. Syst. Evol. 156: 159–176. catch a higher proportion of tourists than hand collecting. Burke, H.R. 1976. Bionomics of Anthonominae weevils. An- Ødegaard (2000b, 2006) found that flower visitors were nual Rev. Entomol. 21: 283–303. significantly more general than both leaf chewers and Dieringer, G., Cabrera R.L., Lara, M., Loya, L. & Reyes- woodborers among phytophagous beetles. Castillo, P. 1999. Beetle pollination and floral ther- The combined effects of large species numbers, high mogenicity in Magnolia tamaulipana (Magnoliaceae). abundance and broad diet breadth across generalist flowers Int. J. Pl. Sci. 160: 64–71. of tropical canopy trees suggests that small- to medium- Endress, P.K. 1994. Diversity and Evolutionary Biology of Tropical Flowers. Cambridge Univ. Press, Cambridge. sized beetles play a crucial role in maintenance of species Erwin, T.L. 1982. Tropical forests: their richness in Coleoptera biodiversity and, hence, forest ecosystem function. and other species. Coleopterists Bull. 36: 74–75. Forel, A. 1910. Das Sinnesleben der Insekten. E. Reinhardt, München. Frame, D. 2003. Generalist flowers, biodiversity and florivory: ACKNOWLEDGEMENTS implications for angiosperm origins. Taxon 52: 681–685. Frame, D. & Durou, S. 2001. Morphology and biology of We are grateful to the Canopy Crane Team at STRI (S.J. Napoleonaea vogelii (Lecythidaceae) flowers in relation Wright, Y. Basset, M. Samaniego, J. Herrera, E. Andrade, and to the natural history of insect visitors. Biotropica 33: O. Saldana) for providing crane access in Panama. L. Krause 458–471. kindly shared valuable information on Tapirira guianensis Gottsberger, G. 1977. Some aspects of beetle pollination in and allowed us to use his photos of flowers. Additionally, Ana the evolution of flowering plants. Pl. Syst. Evol., Suppl. Laccia and Tom Wendt provided helpful advice about the bi- 1: 211–226. Gottsberger, G. 1989. Beetle pollination and flowering rhythm ology of Tapirira guianensis. The descriptions of Nectandra of Annona spp. (Annonaceae) in Brazil. Pl. Syst. Evol. 167: umbrosa and Tapirira guianensis benefited from the expertise 165–187. of Henk van der Werff and John Mitchell, respectively. We Held, D.W. & Potter, D.A. 2004. Floral affinity and benefits thank S. Paton for providing the photo of Nectandra umbrosa of dietary mixing with flowers for a polyphagous scarab, flowers. Several taxonomists kindly identified beetles: W.E. Popillia japonica Newman. Oecologia 140: 312–320. Clark, R.W. Flowers, F.T. Hovore, J. M. Kingsolver, and H.P. Herrera, C.M. 1988. Variation in mutualisms: the spatio-tem- Stockwell. The manuscript benefited from the suggestions and poral mosaic of a pollinator assemblage. Biol. J. Linn. Soc. 35: 95–125. criticisms of three reviewers. The first author received financial Jolivet, P. & Hawkeswood, T.J. 1995. Host-plants of the Chrys- support for this study from the Norwegian Research Council, omelidae of the World. Backhuys Publishers, Leiden. Smithsonian Institution Fellowship Program and Norwegian Kirmse, S., Adis, J. & Morawetz, W. 2003. Flowering events Institute for Nature Research. The second author thanks the and beetle diversity in Venezuela. Pp. 256–265 in: Basset, French government for support from the CAF program. Y., Kitching, R.L., Miller, S. & Novotny, V. (eds.), Ar- thropods of Tropical Forests. Spatio-temporal Dynamics and Resource Use in the Canopy. Cambridge Univ. Press, Cambridge. LITERATURE CITED Krause, L. & Gottsberger, G. 2005. Reproductive features of five insect-pollinated tree species in an Atlantic Rainfor- Barrios, H. 2003. Insect herbivores feeding on conspecific est remnant of northeast Brazil. Pp. 119 in: Del Claro, K. seedlings and trees. Pp. 282–290 in: Basset, Y., Kitching, (ed.), Frontiers in Tropical Biology and Conservation. The R.L., Miller S. & Novotny, V. (eds.), Arthropods of Tropical 2005 Association of Tropical Biology and Conservation Forests. Spatio-temporal Dynamics and Resource Use in Meeting. Universidade Federal de Uberlândia , Uberlândia, the Canopy. Cambridge Univ. Press, Cambridge. Brazil. Basset, Y. 1990. The arboreal fauna of the rainforest tree Magurran, A.E. 2004. 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Appendix. Species list of phytophagous beetles recorded from flowers of Nectandra umbrosa (Nu) and Tapirira guianensis (Tg), and affiliation to guild (G). Nu Tg G Nu Tg G Cerambycidae Amblycerus whiteheadi Kingsolver 5 2 FS Cerambycinae Amblycerus n.sp. 0 1 FS Acyphoderes n.sp. 0 1 F Caryedes godmani (Sharp) 1 0 FS Callichroma viridipes Bates 1 0 F Ctenocolum martiale Kingsolver & White 0 2 FS Coscinedes gracilis Bates 1 1 F Cryptocephalinae Cosmisoma plumicornis Dury 2 0 F Cryptocephalus sp. 1 16 F Gnomidolon laetabile Bates 1 0 F Cryptocephalus sp. 0 2 F Kunaibidion panamensis Giesbert 0 1 F Cryptocephalus sp. 0 3 F Linsleychroma monnei Giesbert 2 0 F Cryptocephalus sp. 0 8 F Megacyllene panamensis Bates 0 1 F Lexiphanes sp. 16 37 F Ommata elegans White 4 0 F Lexiphanes sp. 4 25 F Ommata minuens Giesbert 2 3 F Lexiphanes sp. 101 200 F Ommata n.sp. 0 1 F Lexiphanes sp. 0 2 F Ommata n.sp. 0 4 F Lexiphanes sp. 2 11 F Pandrosus phthisicus (Klug) 2 0 F Lexiphanes sp. 2 0 F Pronuba incognita Hovore & Giesbert 11 0 F Lexiphanes sp. 1 4 F Rhinotragus longicollis Bates 0 3 F Lexiphanes sp. 0 1 F Rhopalophora vercicolor Chevrolat 0 1 F Lexiphanes sp. 1 4 F Terpnissa listropterina Bates 1 1 F Lexiphanes sp. 0 2 F Tetranodus xanthocollis Chemsak 2 4 F Lexiphanes sp. 1 0 F Unidentified genus sp. 1 0 F Chlamisinae Lepturinae ? Chlamisus sp. 3 1 F Megachoriolaus spiniferus (Linsley) 2 0 F Eumolpinae Pseudotypocerus virescens Chemsak & Linsley 2 1 F Brachypnoea sp. 2 12 F Strangalia beltii (Bates) 1 0 F Brachypnoea sp. 0 3 F Strangalia panamensis Giesbert 1 0 F Parachalcoplacis sp. 0 1 F Strangalidium chemsaki Giesbert 3 0 F Spintherophyta sp. 0 7 F Strangalidium kunaium Giesbert 2 1 F Spintherophyta sp. 1 11 F Trichospinthera pilosa (Lefevre) 2 16 F Chrysomelidae Unidentified genus sp. 0 2 F Bruchinae Galerucinae (incl. Alticinae) Acanthoscelides puellus (Sharp) 1 3 FS Calomicrus sp. 1 0 F Acanthoscelides sp. 0 2 FS Calomicrus sp. 1 17 F Acanthoscelides sp. 0 1 FS Diabrotica sp. 36 77 F Amblycerus anosignatus (Chevrolat) 0 1 FS Diabrotica sp. 1 3 F Amblycerus biolleyi (Pic) 1 5 FS Diabrotica sp. 1 0 F Amblycerus cerdanicola Kingsolver 1 0 FS Diabrotica sp. 0 8 F Amblycerus championi Pic 2 13 FS Diabrotica sp. 0 2 F Amblycerus tachigaliae Kingsolver 3 3 FS Diabrotica sp. 3 0 F

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Appendix. Continued. Nu Tg G Nu Tg G Diabrotica sp. 0 1 F Madarus sp. 0 1 F Diabrotica sp. 0 17 F Madarus sp. 1 0 F Diabrotica sp. 3 4 F Pachybaris sp. 1 0 F Diabrotica sp. 0 2 F Parisoschoenus expositus (Champion) 6 10 F Epitrix sp. 3 15 F Parisoschoenus sp. 4 4 F Hypolampis sp. 2 21 F Unidentified genus sp. 7 0 F Hypolampis sp. 0 6 F Unidentified genus sp. 0 1 F Lupraea sp. 5 1 F Unidentified genus sp. 6 0 F Rhinotmetus sp. 2 0 F Unidentified genus sp. 0 2 F Trichaltica sp. 7 1 F Unidentified genus sp. 1 0 F Unidentified genus sp. 46 0 F Unidentified genus sp. 12 1 F Unidentified genus sp. 8 0 F Unidentified genus sp. 18 8 F Unidentified genus sp. 3 1 F Unidentified genus sp. 8 0 F Unidentified genus sp. 2 0 F Unidentified genus sp. 1 0 F Unidentified genus sp. 2 3 F Unidentified genus sp. 1 6 F Unidentified genus sp. 3 0 F Brentidae Unidentified genus sp. 2 2 F Brentinae Unidentified genus sp. 7 2 F Brentus caudatus Herbst 0 1 F Unidentified genus sp. 11 1 F Trachelizinae Unidentified genus sp. 7 0 F Hephebocerus mexicanus Sharp 0 2 F Unidentified genus sp. 10 3 F Paratrachelizus lineatus Sharp 2 1 F Unidentified genus sp. 31 3 F Unidentified genus sp. 0 1 F Unidentified genus sp. 5 0 F Unidentified genus sp. 13 2 F Curculionidae Unidentified genus sp. 13 1 F Curculioninae Unidentified genus sp. 3 0 F Andranthobius palmarum (Champion) 0 1 F Unidentified genus sp. 0 3 F Anthonomus alboscutellatus Champion 1 1 FB Unidentified genus sp. 0 1 F Anthonomus aptus Clark 0 2 FB Unidentified genus sp. 0 1 F Anthonomus arrogans Clark 1 0 FB Unidentified genus sp. 3 0 F Anthonomus occularis Champion 0 1 FB Unidentified genus sp. 2 0 F Anthonomus sp. 1 6 FB Unidentified genus sp. 0 2 F Anthonomus sp. 10 5 F Unidentified genus sp. 2 0 F Anthonomus sp. 23 67 F Unidentified genus sp. 3 0 F Anthonomus sp. 0 1 FB Unidentified genus sp. 6 1 F Loncophorus fusiformis (Champion) 2 1 FB Unidentified genus sp. 14 0 F Loncophorus myrmecodes Clark 0 1 FB Unidentified genus sp. 1 0 F Loncophorus santarosae Clark 0 2 FB Unidentified genus sp. 2 0 F Melexerus sp. 1 1 FB Unidentified genus sp. 0 1 F Phyllotrox sp. 1 1 F Unidentified genus sp. 0 2 F Pseudanthonomus n.sp. 1 0 FB Unidentified genus sp. 0 1 F Tereris ? pilosa 29 2 F Unidentified genus sp. 1 0 F Tereris sp. 1 0 F Unidentified genus sp. 0 2 F Baridinae Unidentified genus sp. 0 1 F Cnagius sp. 1 0 F Cryptorhynchinae Coelonertus nigrirostris Solari 0 1 F Thrasyomus uniformis Champion 2 0 FS Coelonertus sp. 1 0 F Molytinae Coleomerus sp. 2 1 F Conotrachelus aristatus Champion 0 1 FS Cylindrocerus circumlineatus Champion 2 0 F Conotrachelus divrigatus Champion 1 3 FS Eutoxus lacordairei Champion 0 2 F Conotrachelus ? paleatus Champion 1 0 FS Geraeus sp. 0 2 F Conotrachelus punctiventris Champion 2 1 FS Geraeus sp. 1 0 F Conotrachelus sp. 42 1 FS Geraeus sp. 4 0 F Conotrachelus sp. 1 0 F Geraeus serratispinis Champion 0 1 F Conotrachelus sp. 1 2 FS Limnobaris sp. 51 29 F Conotrachelus sp. 3 1 FS Loboderes flavicornis Gyllenhal 1 3 F Conotrachelus sp. 1 0 F Loboderes sulphureiventris Champion 3 27 F Conotrachelus sp. 2 1 FS Loboderes sp. 0 1 F Conotrachelus sp. 3 0 FS Madarus bisignatus Champion 0 1 F Cleogonus rubetra (Fabricius) 1 0 FS Madarus sp. 1 1 F F, general flower visitors; FB, species developing in buds; FS, seed predators.

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